QTL Mapping for Tiller Angle in Rice by Genome-wide Association Analysis

doi:10.16819/j.1001-7216.2024.230904

Abstract

Abstract:

【Objective】Tiller angle is a critical agronomic trait influencing rice yield. Identifying rice tiller angle QTL (genes) and detecting their elite haplotypes can be beneficial for developing ideal rice varieties. 【Method】333 core germplasms from the rice 3K resources were utilized as research materials. These germplasms were cultivated in Yunyuan and Chunhua of Hunan Agricultural University in 2020 and 2022, respectively. Tiller angles of various germplasms were measured during the heading stage. Genome-wide association analysis was conducted using the MLM model of TASSEL 5.2, combined with the genotypes of the germplasms. 【Results】Six QTL for tiller angle were identified on rice chromosomes 2, 5, 6, 9, and 12, designated as qTA2, qTA5, qTA6.1, qTA6.2, qTA9, and qTA12, respectively. These QTL explained phenotypic variation ranging from 6.23% to 16.22%. Notably, qTA9 co-localized with the major QTL TAC1 for tiller angle, while the other five QTL were newly discovered. Candidate gene analysis was conducted for these five QTL. The candidate genes for qTA2 and qTA6.1 were identified as Os02g0817900 and Os06g0682800, respectively. Os02g0817900 encodes a rice cytochrome P450 family protein, while Os06g0682800 encodes a zinc finger domain protein.【Conclusion】This study successfully identified new QTL for tiller angle in rice and analyzed candidate genes, offering valuable insights for the cloning of tiller angle QTL (genes) and genetic improvement of tiller angle in rice.

Key words: rice (Oryza sativa L.), tiller angle, QTL, candidate gene, haplotype

摘要：

【目的】水稻分蘖角度是影响水稻产量的关键农艺性状，挖掘水稻分蘖角度QTL（基因）及其优势单倍型，有助于构建水稻理想株型。【方法】以333份来自水稻3K资源的核心种质为研究材料，于2020年和2022年分别在湖南农业大学耘园基地和春华基地种植，在抽穗期测量分蘖角度，结合基因型，利用TASSEL 5.2的MLM模型进行全基因组关联分析。【结果】共检测到6个分蘖角度QTL位点，分布在水稻2、5、6、9和12号染色体上，分别命名为qTA2、qTA5、qTA6.1、qTA6.2、qTA9和qTA12，这些QTL的表型贡献率为6.23%~16.22%。除了qTA9与分蘖角度主效QTL TAC1共定位外，其余5个QTL均为新的位点。进一步对5个QTL位点进行候选基因分析，初步筛选到qTA2和qTA6.1的候选基因别为Os02g0817900和Os06g0682800，候选基因Os02g0817900编码水稻细胞色素P450家族蛋白，候选基因Os06g0682800编码锌指结构域蛋白。【结论】本研究挖掘到新的水稻分蘖角度相关位点并对候选基因进行了分析，为分蘖角度新QTL（基因）的克隆以及分蘖角度的遗传改良提供参考。

关键词: 水稻, 分蘖角度, QTL, 候选基因, 单倍型

ZHU Yujing, GUI Jinxin, GONG Chengyun, LUO Xinyang, SHI Jubin, ZHANG Haiqing, HE Jiwai. QTL Mapping for Tiller Angle in Rice by Genome-wide Association Analysis[J]. Chinese Journal OF Rice Science, 2024, 38(3): 266-276.

朱裕敬, 桂金鑫, 龚成云, 罗新阳, 石居斌, 张海清, 贺记外. 全基因组关联分析定位水稻分蘖角度QTL[J]. 中国水稻科学, 2024, 38(3): 266-276.

Figures/Tables 9

References 32

[1]	朱亮, 薛蓬勃, 李国强, 黄婧, 金健. 全基因组结合位点分析揭示LAZY1控制水稻分蘖角度的下游调控网络[J]. 基因组学与应用生物学, 2022, 41(7): 1539-1549.
	Zhu L, Xue P B, Li G Q, Huang J, Jin J. Genome-wide binding site analysis of LAZY1 reveals its downstream regulating network in controlling rice tiller angle[J]. Genomics and Applied Biology, 2022, 41(7): 1539-1549. (in Chinese with English abstract)
[2]	黄卫衡, 吕启明, 辛业芸. 水稻分蘖角度的研究进展[J]. 杂交水稻, 2019, 34(3): 1-7.
	Huang W H, Lü Q M, Xin Y Y. Research progress on rice tiller angle[J]. Hybrid Rice, 2019, 34(3): 1-7. (in Chinese with English abstract)
[3]	钱前, 何平, 滕胜, 曾大力, 朱立煌. 水稻分蘖角度的QTLs分析[J]. 遗传学报, 2001(1): 29-32.
	Qian Q, He P, Teng S, Zeng D L, Zhu L H. QTL analysis on rice tiller angle[J]. Journal of Genetics and Genomics, 2001(1): 29-32. (in Chinese with English abstract)
[4]	余传元, 刘裕强, 江玲, 王春明, 翟虎渠, 万建民. 水稻分蘖角度的QTL定位和主效基因的遗传分析[J]. 遗传学报, 2005(9): 948-954.
	Yu C Y, Liu Y Q, Jiang L, Wang C M, Zhai H Q, Wan J M. QTLs mapping and genetic analysis of tiller angle in rice[J]. Journal of Genetics and Genomics, 2005(9): 948-954. (in Chinese with English abstract)
[5]	Yu B S, Lin Z W, Li H X, Li X J, Li J Y, Wang Y H, Zhang X, Zhu Z F, Zhai W X, Wang X K, Xie D X, Sun C Q. TAC1, a major quantitative trait locus controlling tiller angle in rice[J]. Plant Journal, 2007, 52(5): 891.
[6]	Dong H J, Zhao H, Xie W B, Han Z M, Li G W, Yao W, Bai X F, Hu Y, Guo Z L, Lu K, Yang L, Xing Y Z. A novel tiller angle gene, TAC3, together with TAC1 and D2 largely determine the natural variation of tiller angle in rice cultivars[J]. PLoS Genet, 2016, 12(11): e1006412.
[7]	He J W, Shao G N, Wei X J, Huang F L, Sheng Z H, Tang S Q, Hu P S. Fine mapping and candidate gene analysis of qTAC8, a major quantitative trait locus controlling tiller angle in rice (Oryza sativa L.)[J]. PLoS One, 2017, 12(5): e0178177.
[8]	Tan L B, Li X R, Liu F X, Sun X Y, Li C G, Zhu Z F, Fu Y C, Cai H W, Wang X K, Xie D X, Sun C Q. Control of a key transition from prostrate to erect growth in rice domestication[J]. Nature Genetics, 2008, 40(11): 1360.
[9]	Jin J, Huang W, Gao J P, Yang J, Shi M, Zhu M Z, Luo D, Lin H X. Genetic control of rice plant architecture under domestication[J]. Nature Genetics, 2008, 40(11): 1365-1369.
[10]	Zhang W F, Tan L B, Sun H Y, Zhao X H, Liu F X, Cai H W, Fu Y C, Sun X Y, Gu P, Zhu Z F, Sun C Q. Natural variations at TIG1 encoding a TCP transcription factor contribute to plant architecture domestication in rice[J]. Molecular Plant, 2019, 12(8): 1075-1089.
[11]	Okamura M, Hirose T, Hashida Y, Yamagishi T, Ohsugi R, Aoki N. Starch reduction in rice stems due to a lack of OsAGPL1 or OsAPL3 decreases grain yield under low irradiance during ripening and modifies plant architecture[J]. Functional Plant Biology, 2013, 40(11): 1137-1146.
[12]	Huang L Z, Wang W G, Zhang N, Cai Y Y, Liang Y, Meng X B, Yuan Y D, Li J Y, Wu D X, Wang Y H. LAZY2 controls rice tiller angle through regulating starch biosynthesis in gravity-sensing cells[J]. New Phytologist, 2021, 231(3): 1073-1087.
[13]	Sakuraba Y, Piao W, Lim J H, Han S H, Kim Y S, An G, Paek N C. Rice ONAC106 inhibits leaf senescence and increases salt tolerance and tiller angle[J]. Plant Cell Physiology, 2015, 56(12): 2325-2339.
[14]	Wu X R, Tang D, Li M, Wang K J, Cheng Z K. Loose Plant Architecture1, an indeterminate domain protein involved in shoot gravitropism, regulates plant architecture in rice[J]. Plant Physiology, 2013, 161: 317.
[15]	Zhang N, Yu H, Yu H, Cai Y Y, Huang L Z, Xu C, Xiong G S, Meng X B, Wang J Y, Chen H F, Liu G F, Jing Y H, Yuan Y D, Liang Y, Li S J, Smith S M, Li J Y, Wang Y H. A core regulatory pathway controlling rice tiller angle mediated by the LAZY1-dependent asymmetric distribution of auxin[J]. The Plant Cell, 2018, 30(7): 1461-1475.
[16]	Li P J, Wang Y H, Qian Q, Fu Z M, Wang M, Zeng D L, Li B H, Wang X J, Li G Y. LAZY1 controls rice shoot gravitropism through regulating polar auxin transport[J]. Cell Research, 2007, 17(5): 402-410.
[17]	Yoshihara T, Iino M. Identification of the gravitropism-related rice gene LAZY1 and elucidation of LAZY1-dependent and -independent gravity signaling pathways[J]. Plant Cell Physiology, 2007, 48(5): 678.
[18]	Li Z, Liang Y, Yuan Y D, Wang L, Meng X B, Xiong G S, Zhou J, Cai Y Y, Han N P, Hua L K, Liu G F, Li J Y, Wang Y H. OsBRXL4 regulates shoot gravitropism and rice tiller angle through affecting LAZY1 nuclear localization[J]. Molecular Plant, 2019, 12(8): 1143-1156.
[19]	Hu Y, Li S L, Fan X W, Song S, Zhou X, Weng X Y, Xiao J H, Li X H, Xiong L Z, You A Q, Xing Y Z. OsHOX1 and OsHOX28 redundantly shape rice tiller angle by reducing HSFA2D expression and auxin content[J]. Plant Physiology, 2020, 184(3): 1424-1437.
[20]	Li Y, Li J L, Chen Z H, Wei Y, Qi Y H, Wu C Y. OsmiR167a-targeted auxin response factors modulate tiller angle via fine-tuning auxin distribution in rice[J]. Plant Biotechnology Journal, 2020, 18(10): 2015-2026.
[21]	Chen Y N, Fan X R, Song W J, Zhang Y L, Xu G H. Over-expression of OsPIN2 leads to increased tiller numbers, angle and shorter plant height through suppression of OsLAZY1[J]. Plant Biotechnology Journal, 2012, 10(2): 139-149.
[22]	Zhao L, Tan L B, Zhu Z F, Xiao L T, Xie D X, Sun C Q. PAY1 improves plant architecture and enhances grain yield in rice[J]. Plant Journal, 2015, 83(3): 528-536.
[23]	Harmoko R, Yoo J Y, Ko K S, Ramasamy N K, Hwang B Y, Lee E J, Kim H S, Lee K J, Oh D B, Kim D Y, Lee S H, Li Y, Lee S Y, Lee K O. N-glycan containing a core α1, 3-fucose residue is required for basipetal auxin transport and gravitropic response in rice (Oryza sativa)[J]. New Phytologist, 2016, 212(1): 108-122.
[24]	Wang W S, Mauleon R, Hu Z Q, Chebotarov D, Tai S S, Wu Z C, Li M, Zheng T Q, Fuentes R R, Zhang F, Mansueto L, Li Z K, Leung H. Genomic variation in 3,010 diverse accessions of Asian cultivated rice[J]. Nature, 2018, 557(7703): 43-49.
[25]	沈圣泉, 庄杰云, 包劲松, 郑康乐, 夏英武, 舒庆尧. 水稻分蘖最大角度的QTL分析[J]. 农业生物技术学报, 2005(1): 16-20.
	Shen S Q, Zhuang J Y, Bao J S, Zheng K L, Xia Y W, Shu Q Y. QTL analysis of maximum tiller angle in rice[J]. Journal of Agricultural Biotechnology, 2005(1): 16-20. (in Chinese with English abstract)
[26]	Bradbury P J, Zhang Z, Kroon D E, Casstevens T M, Ramdoss Y, Buckler E S. TASSEL: Software for association mapping of complex traits in diverse samples[J]. Bioinformatics, 2007, 23(19): 2633-2635.
[27]	Zhao K, Tung C W, Eizenga G C, Wright M H, Ali M L, Price A H, Norton G J, Islam M R, Reynolds A, Mezey J, McClung A M, Bustamante C D, McCouch S R. Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa[J]. Nature Communications, 2011, 2: 467.
[28]	Bai S H, Hong J, Su S, Li Z K, Wang W S, Shi J X, Liang W Q, Zhang D B. Genetic basis underlying tiller angle in rice by genome-wide association study[J]. Plant Cell Reports, 2022, 41(8): 1707-1720.
[29]	梁彦, 王永红. 水稻株型功能基因及其在育种上的应用[J]. 生命科学, 2016, 28(10): 1156-1167.
	Liang Y, Wang Y H. The genes controlling rice architecture and its application in breeding[J]. Chinese Bulletin: Life Science, 2016, 28(10): 1156-1167. (in Chinese with English abstract)
[30]	陈宗祥, 冯志明, 王龙平, 冯凡, 张亚芳, 马玉银, 潘学彪, 左示敏. 水稻分蘖角基因TAC1的育种应用价值分析[J]. 中国水稻科学, 2017, 31(6): 590-598.
	Chen Z X, Feng Z M, Wang L P, Feng F, Zhang Y F, Ma Y Y, Pan X B, Zuo S M. Breeding potential of rice TAC1 gene for tiller angle[J]. Chinese Journal of Rice Science, 2017, 31(6): 590-598. (in Chinese with English abstract)
[31]	李珍珠, 彭清祥, 邱先进, 徐俊英, 李志新, 刘海洋. 水稻分蘖角度基因TIG1功能性分子标记的开发和应用[J]. 植物遗传资源学报, 2023, 24(3): 808-816.
	Li Z Z, Peng Q X, Qiu X J, Xu J Y, Li Z X, Liu H Y, Development and application of functional molecular marker of rice tiller angle gene TIG1[J]. Journal of Plant Genetic Resources, 2023, 24(3): 808-816. (in Chinese with English abstract)
[32]	Wang L, Xu Y Y, Zhang C, Ma Q B, Joo S H, Kim S K, Xu Z H, Chong K. OsLIC, a novel CCCH-Type zinc finger protein with transcription activationmediates rice architecture via brassinosteroids signaling[J]. PLoS One, 2008, 3(10): e3521.

年份 Year	QTL	染色体 Chr	关联位点 SNP	位置 Position	P值 P value	贡献率 R²(%)
2020	qTA2	2	78 251 484	34 980 561	2.82×10⁻⁵	13.28
	qTA9	9	290 983 508	20 510 958	2.58×10⁻⁵	13.66
	qTA12	12	365 807 909	20 094 246	3.08×10⁻⁶	16.22
2022	qTA5	5	165 535 507	14 410 821	4.36×10⁻⁵	6.23
	qTA6.1	6	208 648 428	27 565 308	1.95×10⁻⁶	8.29
	qTA6.2	6	209 509 442	28 426 322	7.28×10⁻⁶	7.54
	qTA9	9	291 032 810	20 560 260	7.45×10⁻⁸	10.41

年份 Year	QTL	染色体 Chr	关联位点 SNP	位置 Position	P值 P value	贡献率 R²(%)
2020	qTA2	2	78 251 484	34 980 561	2.82×10⁻⁵	13.28
	qTA9	9	290 983 508	20 510 958	2.58×10⁻⁵	13.66
	qTA12	12	365 807 909	20 094 246	3.08×10⁻⁶	16.22
2022	qTA5	5	165 535 507	14 410 821	4.36×10⁻⁵	6.23
	qTA6.1	6	208 648 428	27 565 308	1.95×10⁻⁶	8.29
	qTA6.2	6	209 509 442	28 426 322	7.28×10⁻⁶	7.54
	qTA9	9	291 032 810	20 560 260	7.45×10⁻⁸	10.41

QTL位点 QTL	候选基因 Candidate gene	功能注释 Description
qTA2	Os02g0817600	生长素/吲哚-3-乙酸蛋白
		Auxin/indole-3-acetic acid protein
	Os02g0817900	细胞色素P450家族蛋白
		Cytochrome P450 family protein
qTA6.1	Os06g0663800	叶绿体前体
		Chloroplast precursor
	Os06g0665400	F-box结构域蛋白
		F-box domain containing protein
	Os06g0666500	锌指结构域蛋白
		Zinc finger domain containing protein
	Os06g0679400	Myb转录因子
		Myb-transcription factor
qTA6.2	Os06g0680700	细胞色素P450家族蛋白
		Cytochrome P450 family protein.
	Os06g0682800	锌指结构域蛋白
		Zinc finger domain containing protein
	Os06g0683000	锌指结构域蛋白
		Zinc finger domain containing protein
	Os12g0516900	F-box结构域蛋白
		F-box domain containing protein
qTA12	Os12g0517000	F-box结构域蛋白
		F-box domain containing protein
	Os12g0517100	F-box结构域蛋白
		F-box domain containing protein

QTL位点 QTL	候选基因 Candidate gene	功能注释 Description
qTA2	Os02g0817600	生长素/吲哚-3-乙酸蛋白
		Auxin/indole-3-acetic acid protein
	Os02g0817900	细胞色素P450家族蛋白
		Cytochrome P450 family protein
qTA6.1	Os06g0663800	叶绿体前体
		Chloroplast precursor
	Os06g0665400	F-box结构域蛋白
		F-box domain containing protein
	Os06g0666500	锌指结构域蛋白
		Zinc finger domain containing protein
	Os06g0679400	Myb转录因子
		Myb-transcription factor
qTA6.2	Os06g0680700	细胞色素P450家族蛋白
		Cytochrome P450 family protein.
	Os06g0682800	锌指结构域蛋白
		Zinc finger domain containing protein
	Os06g0683000	锌指结构域蛋白
		Zinc finger domain containing protein
	Os12g0516900	F-box结构域蛋白
		F-box domain containing protein
qTA12	Os12g0517000	F-box结构域蛋白
		F-box domain containing protein
	Os12g0517100	F-box结构域蛋白
		F-box domain containing protein

基因 Gene		单倍型1/种质数 Hap1/Accession number	单倍型2/种质数 Hap2/Accession number	单倍型3/种质数 Hap3/Accession number
Os02g0817900	AACGGACAAT/51	AACGGGCAAT/33	TGATGACGGCGC/81
Os06g0682800		GGGATG/77	GATACCA/70
Os06g0663800		ATGGCCCGC/46	ATTGCCCGC/41	GCGAATTAT/74
Os02g0817600		CGATCC/56	CGCGTT/25	GACGTC/50
Os06g0680700		AATTCAATGAAGCTGAAG/78	GGGGGGGCAGGCGCTGGT/79